Adding pieces to the puzzling plant nuclear envelope
Introduction
In eukaryotic cells, the nuclear envelope (NE) separates the nucleoplasm from the cytoplasm. The gateways for macromolecules through the NE are the nuclear pore complexes (NPCs), large multiprotein complexes of an eightfold symmetry embedded in the NE double membranes. Proteins and RNAs traffic through the NPCs, enabled by the interacting activities of the nuclear transport receptors (the karyopherins), the NPC proteins (Nups) and the elements of the Ran cycle (see Box 1, Figure I). In the animal and yeast fields, a combination of proteome, interactome, functional, and modeling studies are increasingly refining our understanding of the NPC (reviewed in [1]). Plant NE and NPC research is by comparison less advanced, in part based on the old expectation in the field that not much new could be learned by studying such a likely conserved cellular system. Over the past years, however, numerous reports have demonstrated that firstly, plants do not simply possess a carbon copy of the well-known animal and yeast systems [2, 3, 4, 5], and secondly, that both in plants [6] and in animals [7], NE and NPC biology hold more clues about regulation at the cellular and organismal level than previously anticipated. This renewed interest within the plant community is reflected in the number of exciting reports that have appeared in the past 18 months. They deal with the refined ultrastructure of the NE and NPC, with the discovery of novel NE components, and, importantly, with novel roles and fates of NE-associated and NPC-associated proteins during plant mitosis and cytokinesis (Table 1). Here, we focus on these new studies, while referring to recent reviews for plant work before the discussed time period [6, 8].
Section snippets
Ion channels
In animal cells, Ca2+ channels in the NE and ER are known to cause Ca2+ oscillations at the nuclear periphery. The channels are activated by secondary messengers such as IP3, which is liberated by phospholipase C [9]. In plants, Nod factor production by rhizobia causes two genetically separable Ca2+ responses, a rapid influx of calcium into root hair tips, and a slower appearance of calcium oscillations in the perinuclear region [10]. CASTOR and POLLUX were identified in mutant screens in Lotus
Conclusions
Much progress has been made in the past two to three years in determining components of the plant NPC and NE and in describing their contribution to diverse plant signaling processes (reviewed in [6]). In the meantime, however, the field has all but exploded in yeast and animal models, including precise structural models of the NPC, biophysical understanding of nucleocytoplasmic transport, the role of the NE in gene regulation and human disease, and the emerging evidence that nucleocytoplasmic
References and recommended reading
Papers of particular interest published within the period of review have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgement
Funding of our lab's research in this field by the National Science Foundation is greatly acknowledged.
References (57)
- et al.
Structure, dynamics and function of nuclear pore complexes
Trends Cell Biol
(2008) - et al.
Anchorage of plant RanGAP to the nuclear envelope involves novel nuclear-pore-associated proteins
Curr Biol
(2007) - et al.
The nuclear pore and plant development
Curr Opin Plant Biol
(2009) - et al.
The nuclear pore comes to the fore
Trends Plant Sci
(2008) - et al.
Calcium spiking in plant root hairs responding to Rhizobium nodulation signals
Cell
(1996) - et al.
Nuclear membrane ion channels mediate root nodule development
Trends Plant Sci
(2009) - Graumann K, Runions J, Evans D. Characterization of SUN domain proteins at the plant nuclear envelope. Plant J. Epub...
- et al.
The mechanism of spindle assembly: functions of Ran and its target TPX2
J Cell Biol
(2004) - et al.
Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation
J Cell Biol
(2003) - et al.
The molecular architecture of the nuclear pore complex
Nature
(2007)
Composition of the plant nuclear envelope: theme and variations
J Exp Bot
Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling
Curr Genet
Two distinct, interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP
Plant Cell
The role of nuclear pores in gene regulation, development and disease
EMBO Rep
New aspects of nuclear calcium signalling
J Cell Sci
Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots
Nature
Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis
Plant Cell
Nuclear regulators with a second home in organelles
Trends Plant Sci
SUN-domain and KASH-domain proteins during development, meiosis and disease
Cell Mol Life Sci
Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins
Plant J
Structure of the nuclear pore in higher plants
Nature
Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells
Plant J
Cell-cycle-dependent dynamics of nuclear pores: pore-free islands and lamins
J Cell Sci
Dynamics of nuclear pore distribution in nucleoporin mutant yeast cells
J Cell Biol
NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development
Plant Cell
The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling
Plant Physiol
Purification and immunological detection of pea nuclear intermediate filaments: evidence for plant nuclear lamins
J Cell Sci
Immunological characterization of lamins in the nuclear matrix of onion cells
J Cell Sci
Cited by (29)
New insights into the dynamics of plant cell nuclei and chromosomes
2013, International Review of Cell and Molecular BiologyCitation Excerpt :NPCs mediate the transport of molecules between the nucleoplasm and cytoplasm. While small molecules including ions, water, sugars, and low-molecular weight proteins can passively diffuse across NPCs (Wente and Rout, 2010), macromolecules larger than 25–40 kDa are considered to require cargo proteins, for example, importin and exportin, to pass through the NPC (Meier and Brkljacic, 2009), indicating that the NPC properly transport macromolecules (Tran and Wente, 2006). The NPC structure is widely conserved among eukaryotes from yeast to human (Alber et al., 2007; Beck et al., 2007; Brohawn et al., 2009).
Dynamic behavior of double-membrane-bounded organelles in plant cells
2011, International Review of Cell and Molecular BiologyCitation Excerpt :At present, KASH proteins are thought to function in multiple ways to position nuclei; they mediate nuclear anchorage in C. elegans and mammals, nuclear migration via centrosome attachment in D. melanogaster and C. elegans, nuclear migration without centrosome in C. elegans, and association of nuclei with intermediate filaments in mammals (Starr, 2009). SUN homologs of A. thaliana, AtSUN1 and AtSUN2, have been partially characterized (Graumann et al., 2010; Meier and Brkljacic, 2009). Both AtSUN1 and AtSUN2 seemed to be localized at the nuclear envelope, especially the inner nuclear membrane (Graumann et al., 2010), which is consistent with the localization of SUN proteins in the yeast and animals (Starr, 2009).
Ion channels at the nucleus: Electrophysiology meets the genome
2010, Molecular PlantCitation Excerpt :The central channel has an average diameter of ∼9–10 nm (Bootman et al., 2009) but can expand to accommodate particles up to ∼39 nm in diameter (Panté and Kann, 2002). The conventional view is that the central channel permits passive diffusion of ions, small molecules and proteins (<30–40 kD) and facilitates selective transport of larger proteins and nucleoprotein complexes that carry a signal sequence (Hetzer and Wente, 2009; Meier and Brkljacic, 2009b). FG-NUPs contribute to the size-selectivity of the central channel, perhaps by forming a hydrogel-like meshwork (Frey et al., 2006; Mohr et al., 2009), although other models have also been proposed (Terry and Wente, 2009).
Protein-protein interactions in plant antioxidant defense
2022, Frontiers in Plant ScienceA nuclear import pathway exploited by pathogenic noncoding RNAs
2022, Plant Cell